Complete Mitochondrial Genome of the Western Capercaillie Tetrao Urogallus (Phasianidae, Tetraoninae)

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Zootaxa 4550 (4): 585–593 ISSN 1175-5326 (print edition) https://www.mapress.com/j/zt/ Article ZOOTAXA Copyright © 2019 Magnolia Press ISSN 1175-5334 (online edition) https://doi.org/10.11646/zootaxa.4550.4.9 http://zoobank.org/urn:lsid:zoobank.org:pub:12E18262-0DCA-403A-B047-82CFE5E20373

Complete mitochondrial genome of the Western Capercaillie Tetrao urogallus (Phasianidae, Tetraoninae)

GAËL ALEIX-MATA1,5, FRANCISCO J. RUIZ-RUANO2, JESÚS M. PÉREZ1, MATHIEU SARASA3 & ANTONIO SÁNCHEZ4 1Department of Animal and Plant Biology and Ecology, Jaén University, Campus Las Lagunillas, E-23071, Jaén, Spain. E-mail: [email protected] 2Departamento de Genética, Facultad de Ciencias, Universidad de Granada, Avda. Fuentenueva, 18071 Granada, Spain. 3BEOPS, 1 Esplanade Compans Caffarelli, 31000 Toulouse, France 4Department of Experimental Biology, Jaén University, Campus Las Lagunillas, E-23071, Jaén, Spain 5Corresponding author Gaël Aleix-Mata: [email protected] ORCID: 0000-0002-7429-4051 Francisco J. Ruíz-Ruano: [email protected] ORCID: 0000-0002-5391-301X Jesús M. Pérez: [email protected] ORCID: 0000-0001-9159-0365 Mathieu Sarasa: [email protected] ORDCID: 0000-0001-9067-7522 Antonio Sánchez: [email protected] ORCID: 0000-0002-6715-8158

Abstract

The Western Capercaillie (Tetrao urogallus) is a galliform bird of boreal climax forests from Scandinavia to eastern Sibe- ria, with a fragmented population in southwestern Europe. We extracted the DNA of T. urogallus aquitanicus and obtained the complete mitochondrial genome (mitogenome) sequence by combining Illumina and Sanger sequencing sequence data. The mitochondrial genome of T. urogallus is 16,683 bp long and is very similar to that of Lyrurus tetrix (16,677 bp). The T. urogallus mitogenome contains the normal 13 protein-coding genes (PCGs), 22 transfer RNAs, 2 ribosomal RNAs, and the control region. The number, order, and orientation of the mitochondrial genes are the same as in L. tetrix and in other species of the same and other bird families. The three domains of the control region contained conserved sequences

(ETAS; CSBs), boxes (F, E, D, C, B, BS box), the putative origin of replication of the H-strand (OH) and bidirectional promoters of translation (LSP/HSP).

Key words: control region, mitogenome, Phasianidae, Tetrao urogallus

Introduction

The Order Galliformes contains about 290 species, approximately 10% of which are listed as globally Endangered or Critically Endangered (del Hoyo et al. 1994; Hosner et al. 2016; IUCN 2017). Traditionally, the species of this order are divided into seven families: Megapodiidae, Cracidae, Odontophoridae, Numididae, Phasianidae, Meleagrididae, and Tetraonidae (del Hoyo et al. 1994). The family Phasianidae, with more than 150 species, is distributed throughout the world (Johnsgard 1986; Fuller & Garson 2000; Fuller et al. 2000). The genus Tetrao (subfamily Tetraoninae) includes two extant species, T. urogallus Linnaeus and T. urogalloides Middendorff. The Western Capercaillie (Tetrao urogallus) is the best-known species of this genus and is found typically in boreal climax forests from Scandinavia to eastern Siberia, but also in a fragmented population in southwestern Europe (Storch 2007). In this latter region, it is present in the Pyrenees (France, Andorra and Spain) and in the Cantabrian Mountains of Spain (de Juana 1994). Using morphological characteristics, up to 12 T. urogallus subspecies have been described (de Juana 1994), although some are not well supported by mitochondrial DNA analyses (Liukkonen-Anttila et al. 2004). The two capercaillie subspecies of southwestern Europe, T. urogallus aquitanicus Ingram of the Pyrenees and T. urogallus cantabricus Castroviejo of the Cantabrian Mountains, are both considered Threatened in small-scale assessments (Canut et al. 2004; Obeso 2004; Rodríguez- Muñoz et al. 2007; Charra & Sarasa 2018).

Accepted by P. Rasmussen: 12 Nov. 2018; published: 29 Jan. 2019 585 Although scientific information on demography over the last 20 years is scarce (Gée et al. 2018), the biology and ecology of T. urogallus is quite well-known, and information is available on reproduction, population and/or subspecific variations, and genetics (Rodríguez-Muñoz et al. 2007; Mollet et al. 2015; Fameli et al. 2017; Kowalczyk et al. 2017; Rutkowski et al. 2017). Genetic studies have analyzed several DNA markers, most of them mitochondrial DNA sequences [12s rRNA, 16s rRNA, cytochrome oxidase I (CoI), cytochrome B (CytB), control region (D-loop)] and several microsatellites (Segelbacher et al. 2008; Lucchini et al. 2001; Dimcheff et al. 2002; Kerr et al. 2009; Pérez et al. 2011). At present, a complete mitogenome sequence is not available for either of the two Tetrao species. However, the mitogenome of the Black Grouse, Lyrurus tetrix Linnaeus, a closely related species previously included in genus Tetrao, has been described (Li et al. 2016). In this study, we sequenced and described the complete mitochondrial genome of T. urogallus aquitanicus, which we then compared with that of L. tetrix.

Materials and methods

DNA extraction, sequencing, and mitogenome assemblage. Genomic DNA was extracted from liver tissue of an individual of T. urogallus aquitanicus using the DNeasy Blood & Tissue Kit (Qiagen). For genome sequencing, 3 µg of genomic DNA were used for the construction of a library with 750 bp fragments. This library was used in Illumina® Hiseq™ 2000 paired-end sequencing with 100 bp reads. Two Gbp of sequences were obtained (coverage about 1.5X). We assembled the sequence for the T. urogallus mitogenome using the MITObim v1.8 program (Hahn et al. 2013) with the "--quick" option and with the default mismatch of 15%. For this purpose, we randomly selected one million read pairs with seqTK (https://github.com/lh3/seqtk) and used as a reference the mitogenome of Lyrurus tetrix (accession number KF955638.1; Li et al. 2016). A region containing the D-loop and the gene Nd6 of the mitochondrial genome was not recovered completely and so was amplified by PCR using the same T. urogallus sample and sequenced. For PCR amplification the primer pair Pro+ (5’- ACCATCAGCACCCAAAGCTG-3’) and Phe- (5’-AAGCATTTTCAGTGCTTTGCTT-3’) were used (Haring et al. 2000). Sequences were analyzed with Bioedit (version 7.0.9.0) (http://www.mbio.ncsu.edu/BioEdit/ bioedit.html). The annotation of the T. urogallus mitogenome was fulfilled using web-based services MITOS (http://mitos.bioinf.uni-leipzig.de/help.py) (Bernt et al. 2013) and tRNA scan-SE (http://lowelab.ucsc.edu/ tRNAscan-SE/) (Lowe & Eddy 1997). The annotations of protein coding genes (PCGs), transfer RNAs (tRNAs) and rRNA genes were refined by comparing manually with the L. tetrix mitogenome (Li et al. 2016). The circular drawing of the mitogenome was carried out using the OrganellarGenomeDRAW tools (http://ogdraw.mpimp- golm.mpg.de/) (Lohse et al. 2013).

Results and discussion

Genome organization and gene arrangement. The mitochondrial genome of T. urogallus was assembled and submitted to GenBank (accession number MG583885). It is composed of 13 protein-coding genes (PCGs), two ribosomal RNA genes (rRNAs), 22 transfer RNA genes (tRNAs), and the non-coding region (D-loop) (Table 1, Fig. 1). The mitogenome of T. urogallus is 16,683 bp long, similar to the L. tetrix mitogenome of 16,677 bp (Li et al. 2016); both have a percentage of identity of 94.70%. The total base composition of the T. urogallus mitochondrial genome is 30.15% A, 30.55% C, 13.62% G, and 25.67% T; the A-T content is 55.82%, which is also very similar to the L. tetrix base composition and A-T content (30.37% A, 30.42% C, 13.38% G, 25.83% T; A-T content 56.20%) (Li et al. 2016). Protein coding genes (PCGs). The total length of the 13 PCGs of T. urogallus was 11,392 bp (68.23% of the total length of the mitogenome); the similarities with the 13 PCGs of L. tetrix is very high (varying between 96.10% of the Nd1 and 92.66% of the Nd6) (Table 2). The main differences affect the Nd6 gene of L. tetrix, which has an 18-bp nucleotide deletion and gives rise to a smaller protein; this deletion is absent from the same gene in T. urogallus and other Phasianidae species (Nishibori et al. 2001; Guan et al. 2010; Kan et al. 2010; Shen et al. 2010; Li et al. 2016). In addition, as in other bird species including L. tetrix, the Nd3 gene of T. urogallus has an extra nucleotide in position 174 (mitogenome nt 10,855, C) that is not translated (Mindell et al. 1998; Li et al. 2016).

586 · Zootaxa 4550 (4) © 2019 Magnolia Press ALEIX-MATA ET AL. TABLE 1. Gene organization of the Tetrao urogallus mitogenome. Gene Strand Nucleotide positions Size (bp) Anticodon Intergenic nucleotide D-loop H 1–1141 1141 tRNAPhe H 1142–1208 67 TTC 12S rRNA H 1209–2171 963 tRNAVal H 2172–2244 73 GTA 16S rRNA H 2245–3858 1614 tRNALeu (uur) H 3859–3932 74 TTA Nd1 H 3944–4918 975 11 tRNAIle H 4919–4992 74 ATC tRNAGln L 4999–5069 71 CAA 6 tRNAMet H 5069–5137 69 ATG -1 Nd2 H 5138–6176 1039 tRNATrp H 6177–6253 77 TGA tRNAAla L 6260–6328 69 GCA 6 tRNAAsn L 6333–6405 73 AAC 4 tRNACys L 6408–6473 66 TGC 2 tRNATyr L 6473–6543 71 TAC -1 COI H 6545–8095 1551 1 tRNASer (ucn) L 8087–8161 75 TCA -9 tRNAAsp H 8164–8232 69 GAC 2 COII H 8234–8917 684 1 tRNALys H 8919–8989 71 AAA 1 Atp8 H 8991–9155 165 1 Atp6 H 9146–9829 684 -10 COIII H 9829–10,612 784 -1 tRNAGly H 10,614–10,681 68 GGA 1 Nd3 H 10,682–11,033 352 tRNAArg H 11,035–11,103 69 CGA 1 Nd4L H 11,104–11,400 297 Nd4 H 11,394–12,771 1378 -7 tRNAHis H 12,772–12,840 69 CAC tRNASer H 12,842–12,906 65 AGC 1 tRNALeu H 12,908–12,978 71 CTA 1 Nd5 H 12,979–14,796 1818 CytB H 14,801–15,943 1143 4 tRNAThr H 15,946–16,014 69 ACA 2 tRNAPro L 16,017–16,086 70 CCA 2 Nd6 L 16,093- 16,614 522 6 tRNAGlu L 16,616–16,683 68 GAA 1

Intergenic nucleotide: denotes the number of overlapping nucleotides (negative values) or the number of spacer nucleotides (positive values) between two consecutive genes.

Most of the 13 PCGs of T. urogallus started with the ATG start codon, the exception being CoI, which has GTG as the start codon. In L. tetrix, both the CoI and Nd5 genes also start with GTG. In both these species, the genes Nd1, CoII, Atp8, Atp6, Nd3, Nd4L, Nd5, and CytB all have TAA stop codons, while gene Nd6 has a TAG

WESTERN CAPERCAILLIE TETRAO UROGALLUS Zootaxa 4550 (4) © 2019 Magnolia Press · 587 stop codon, CoI has AGG and Nd2, CoIII, and Nd4 have incomplete T-- stop codons (Table 2). Incomplete stop codons (T--), which occur in three PCGs, are common in mitogenomes and may be completed by the polyadenylation of the 3’-end of the mRNA after transcription (Ojala 1981; Mouchaty et al. 2000). There were 3795 codons for the 13 PCGs, excluding incomplete termination codons; the most frequently occuring amino acid was Leu (13.6%).

FIGURE 1. Map of the mitochondrial genome of Tetrao urogallus. Genes encoded by the heavy strand are shown outside the circle, while those encoded by the light strand are shown inside the circle.

tRNA and rRNA genes. All 22 tRNAs sequences have similar lengths, which is 1,547 bp and 1,546 bp for T. urogallus and L. tetrix, respectively, and an identity percentage of 96.82% when comparing the mitogenomes of both species. The size of the tRNAs varied between 65 bp for tRNASer and tRNACys, and 77 bp for the tRNATrp (Table 1). As in other mitogenome studies of species from the same family, most of the tRNA genes are located on the heavy strand, the exceptions being eight (tRNAGln / tRNAAla / tRNAAsn / tRNACys / tRNATyr / tRNASer / tRNAPro / tRNAGlu) that are located on the light strand (Table 1) (Li et al. 2016; Chen et al. 2017). Three clusters of tRNAs— IQM, WANCY, and HSL—are present in the mitogenome of the two species, as has previously been described in other avian species (Chen et al. 2017) (Fig. 1).

588 · Zootaxa 4550 (4) © 2019 Magnolia Press ALEIX-MATA ET AL. TABLE 2. Comparison between the sequences 13 PCGs of T. urogallus and L. tetrix mitogenomes. Gene Length (bp) AT Content % Identity Start/Stop codons Protein length T. uro L. tet T. uro L. tet T. uro L. tet T. uro L. tet Nd1 975 975 54.15 54.05 96.10 ATG/TAA ATG/TAA 324 324 Nd2 1039 1039 58.52 58.81 92.88 ATG/T-- ATG/T-- 346 346 COI 1551 1551 54.16 54.93 94.62 GTG/AGG GTG/AGG 516 516 COII 684 684 56.29 55.26 96.05 ATG/TAA ATG/TAA 227 227 Atp8 165 165 60.61 59.39 92.12 ATG/TAA ATG/TAA 54 54 Atp6 684 684 55.41 55.26 94.44 ATG/TAA ATG/TAA 227 227 COIII 784 784 54.59 54.85 95.54 ATG/T-- ATG/T-- 261 261 Nd3* 352 352 52.27 54.26 93.73 ATG/TAA ATG/TAA 116 116 Nd4L 297 297 55.89 55.56 93.60 ATG/TAA ATG/TAA 98 98 Nd4 1378 1378 56.31 57.33 93.69 ATG/T-- ATG/T-- 459 459 Nd5 1818 1818 55.83 56.88 93.67 ATG/TAA GTG/TAA 605 605 CytB 1143 1143 53.37 54.24 93.61 ATG/TAA ATG/TAA 380 380 Nd6 522 504 53.64 52.78 92.66 ATG/TAG ATG/TAG 173 167 Total 11,392 11,374 55.26 55.71 94.18 *Nd3 has one additional C that is not translated

In T. urogallus, the 12s rRNA and 16s rRNA genes are situated between the tRNAPhe and the tRNALeu. They are separated by the tRNAVal and have a length of 963 bp and 1614 bp, respectively. This situation is the same in L. tetrix but with respective lengths of 971 bp and 1611 bp (Li et al. 2016). The 12s rRNA and 16s rRNA of both species have identity percentages of 97.51% and 94.97%, respectively. In addition, the 12s rRNA and 16s rRNA in the two species are slightly A-T rich (54.83% in T. urogallus and 54.38% in L. tetrix 12s rRNA; 56.13% in T. urogallus; and 56.36% in L. tetrix 16s rRNA), as in other Phasianidae (e.g., Bonasa sewerzowi Przevalski) (Li et al. 2014) and other avian species (Chen et al. 2017; Shi et al. 2017). Control region. The mtDNA CR is mainly involved in the replication, termination, and transcription of the mitochondrial genome. The control region (D-loop) is the most variable region between the two mitogenomes that have a sequence identity in T. urogallus and L. tetrix of 93.60%, a length of 1,141 bp and 1,147 bp, and a A-T content of 58.98% and 59.98%, respectively. Huang & Ke (2014) found that the length of the control region (about 1150 bp) is relatively well-conserved in Phasianidae. We aligned the control region of both mitogenomes and identified the three domains —domain I, the central conserved domain II, and domain III (positions 1–315, 316– 782, and 783–1148 respectively; Fig. 2) —and several other conserved regions, as in other Phasianidae species (Randi & Lucchini 1998; Huang & Ke 2014). Domain I contained two conserved extended termination-associated sequences, ETAS1 (62–121) and ETAS2 (108–167), as well as the shorter TAS (TATAT or TACAT motifs) that can form stable secondary structures (Fig. 2). At the beginning of this domain a C-stretch interrupted by three Ts (goose hairpin) conserved in Galliformes and Anseriformes is able to form a hairpin structure along with a string of guanines, located a short distance downstream (Ruokonen & Kvist 2002; Buehler & Baker 2003). Two TCCC motifs are found in both T. urogallus and L. tetrix; in other species three such motifs have been described and are linked to the termination of H-strands in mammalian and bird D-loops (Douzery & Randi 1997; Randi & Lucchini 1998). Finally, two CSB-1-like sequences exist in both these grouse species and also in other avian species, including other Phasianidae (Fig. 2) (Randi & Lucchini 1998; Yang et al. 2015). In Domain II, five highly conserved sequence boxes were localized and identified as boxes F, E, D, C, and B (Fig. 2). The four first boxes (but not the B-box) were also identified in Phasianidae by Randi & Lucchini (1998) and Huang & Ke (2014). We identified the B-box by comparison with the sequences described by Ruokonen & Kvist (2002) in their study of the avian mitochondrial control region. Furthermore, we identified a very well- conserved bird similarity box (BS Box) (Fig. 2), which has identical sequences in several analyzed avian groups

WESTERN CAPERCAILLIE TETRAO UROGALLUS Zootaxa 4550 (4) © 2019 Magnolia Press · 589 (Ruokonen & Kvist 2002; Buehler & Baker 2003; Li et al. 2014). The function of these six boxes is not yet clear, although they could be related to D-loop formation and H-strand replication (Yang et al. 2015). In Domain III, we identified the conserved sequence blocks 1 and 3 (CSB-1 and CSB-3) (Fig. 2) but were not able to identify conserved sequence block 2 (CSB-2). In previous studies in the Domain III of Phasianidae and other avian groups CSB-1 was identified, although with considerable sequence variation; however, the conserved sequences CSB-2 and CSB-3 were not found (Baker & Marshall 1997; Huang & Ke 2014). The characteristic motif of CSB-1 is GACATA, identical to several vertebrate mtDNA CSB-1sequences (Sbisà et al. 1997), while that of CBS-3 is a poly(C) track (Zhang et al. 2009). These sequences (CSB) are involved in potential secondary structures and have been proposed as regulatory signals for the processing of the RNA primers for H?strand replication (Sbisà et al. 1997). Domain III also included a poly(C) sequence, which was similar to a replication initiation of a mammalian heavy chain (OH), and the bidirectional promoters of translation (LSP/HSP) also identified in other birds (L’Abbé et al. 1991) including Phasianidae species (Randi & Lucchini 1998; Li et al. 2014), as well as a long track of poly(T) between CSB-1 and LSP and HSP bidirectional promoters (Fig. 2).

FIGURE 2. Aligned nucleotide sequences of the control region of Tetrao urogallus (T.uro) and Lyrurus tetrix (L.tet). Dots indicate the identity of the nucleotides and dashes the indels. The limits between Domains I to III are indicated by arrows. Domain I: The putative ends of H-strand DNA synthesis at TCCC motifs are shown in italics and highlighted in gray. The stem and loop of the goose hairpin are underlined with double lines and dots, respectively. Sequences ETAS1 (62–121) and ETAS2 (108–167) sequences are both included in a single large box, with the overlap nucleotides in gray and TATAT and TACAT sequences underlined. The CSB-1-like motifs are double-underlined. Domain II: The six conserved blocks identified F, E, D, C,

B, and Bird Similarity (BS) box are in boxes. Domain III: The putative origin of the replication of the H-strand (OH), CSB1, CSB-3, and the sequence corresponding to the avian bidirectional LSP/HSP promoters are also shown in boxes.

Acknowledgements

This work and the research activities of GAM are funded by the Fédération Nationale des Chasseurs (France), Fédération Départementale des Chasseurs de l’Ariège (France), Fédération Départementale des Chasseurs des Hautes Pyrénées (France) (project FNC-PSN-PR16-2014), the Fundación para la Conservación del Quebrantahuesos (Spain) (project FCQ-UJ-2017), and the Government of Andorra (project GA-UJ-2017). The research activities of authors are partially funded by the PAIDI, Junta de Andalucía (RNM-118 group). The authors express their gratitude to Edgar Madrenys for the picture of the T. urogallus in Figure 1.

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